Mutations in PROSC Disrupt Cellular Pyridoxal Phosphate Homeostasis and Cause Vitamin-B6-Dependent Epilepsy

American Journal of Human Genetics

Volumn 99, Issue 6, 2016, Pages 1325-1337

  Darin, Niklas ^a   Reid, Emma ^b   Prunetti, Laurence ^c   Samuelsson, Lena ^d   Husain, Ralf A ^e   Wilson, Matthew ^b   El Yacoubi, Basma ^c,l   Footitt, Emma ^f   Chong, W K ^f   Wilson, Louise C ^f   Prunty, Helen ^f   Pope, Simon ^g   Heales, Simon ^b,f,g   Lascelles, Karine ^h   Champion, Mike ^h   Wassmer, Evangeline ⁱ   Veggiotti, Pierangelo ^j,k   de Crécy Lagard, Valérie ^c   Mills, Philippa B ^b   Clayton, Peter T ^b  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF FLORIDA   (United States)

^d SAHLGRENSKA UNIVERSITY HOSPITAL   (Sweden)

^e JENA UNIVERSITY HOSPITAL   (Germany)

^f GREAT ORMOND STREET HOSPITAL   (United Kingdom)

^g National Hospital   (United Kingdom)

^h ST THOMAS HOSPITAL   (United Kingdom)

ⁱ BIRMINGHAM CHILDREN S HOSPITAL   (United Kingdom)

^j C MONDINO NATIONAL NEUROLOGICAL INSTITUTE   (Italy)

^k UNIVERSITY OF PAVIA   (Italy)

^l UNIVERSITY OF FLORIDA   (United States)

more..

Author keywords

developmental delay; epilepsy; homeostasis; microcephaly; PROSC; pyridoxal 5 phosphate; pyridoxine; treatment; vitamin B6; YggS

Indexed keywords

APOENZYME; GENOMIC DNA; PYRIDOXAL 5 PHOSPHATE; PYRIDOXINE; CARNOSINE; HOMOCARNOSINE; PROLINE; PROSC PROTEIN, HUMAN; PROTEIN;

ADOLESCENT; ARTICLE; BACTERIAL GROWTH; CELL DISRUPTION; CEREBROSPINAL FLUID ANALYSIS; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME INACTIVATION; EPILEPSY; EPILEPTOGENESIS; ESCHERICHIA COLI; FEMALE; FIBROBLAST; FIBROBLAST CULTURE; GENE; GENE MAPPING; GENETIC TRANSFECTION; GROWTH INHIBITION; HOMOZYGOSITY; HUMAN; HUMAN CELL; INFANT; MALE; NONHUMAN; NONSENSE MUTATION; PRESCHOOL CHILD; PRIORITY JOURNAL; PROSC GENE; PYRIDOXINE DEFICIENCY; SCHOOL CHILD; SEQUENCE ANALYSIS; VITAMIN BLOOD LEVEL; VITAMIN METABOLISM; ANALOGS AND DERIVATIVES; BLOOD; CELL CULTURE; EXOME; GENETICS; HOMEOSTASIS; HOMOZYGOTE; METABOLISM; MUTATION; PEDIGREE;

ADOLESCENT; CARNOSINE; CELLS, CULTURED; CHILD; CHILD, PRESCHOOL; EPILEPSY; EXOME; FEMALE; FIBROBLASTS; HOMEOSTASIS; HOMOZYGOTE; HUMANS; INFANT; MALE; MUTATION; PEDIGREE; PROLINE; PROTEINS; PYRIDOXAL PHOSPHATE; VITAMIN B 6;

EID: 85004081533     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2016.10.011     Document Type: Article

References (37)

1. 1 Whittaker, J.W., Intracellular trafficking of the pyridoxal cofactor. Implications for health and metabolic disease. Arch. Biochem. Biophys. 592 (2016), 20–26.
2. 2 Waymire, K.G., Mahuren, J.D., Jaje, J.M., Guilarte, T.R., Coburn, S.P., MacGregor, G.R., Mice lacking tissue non-specific alkaline phosphatase die from seizures due to defective metabolism of vitamin B-6. Nat. Genet. 11 (1995), 45–51.
3. 3 Belachew, D., Kazmerski, T., Libman, I., Goldstein, A.C., Stevens, S.T., Deward, S., Vockley, J., Sperling, M.A., Balest, A.L., Infantile hypophosphatasia secondary to a novel compound heterozygous mutation presenting with pyridoxine-responsive seizures. JIMD Rep. 11 (2013), 17–24.
4. 4 Gachon, F., Fonjallaz, P., Damiola, F., Gos, P., Kodama, T., Zakany, J., Duboule, D., Petit, B., Tafti, M., Schibler, U., The loss of circadian PAR bZip transcription factors results in epilepsy. Genes Dev. 18 (2004), 1397–1412.
5. 5 Mills, P.B., Surtees, R.A., Champion, M.P., Beesley, C.E., Dalton, N., Scambler, P.J., Heales, S.J., Briddon, A., Scheimberg, I., Hoffmann, G.F., et al. Neonatal epileptic encephalopathy caused by mutations in the PNPO gene encoding pyridox(am)ine 5′-phosphate oxidase. Hum. Mol. Genet. 14 (2005), 1077–1086.
6. 6 Mills, P.B., Camuzeaux, S.S., Footitt, E.J., Mills, K.A., Gissen, P., Fisher, L., Das, K.B., Varadkar, S.M., Zuberi, S., McWilliam, R., et al. Epilepsy due to PNPO mutations: genotype, environment and treatment affect presentation and outcome. Brain 137 (2014), 1350–1360.
7. 7 Mills, P.B., Struys, E., Jakobs, C., Plecko, B., Baxter, P., Baumgartner, M., Willemsen, M.A., Omran, H., Tacke, U., Uhlenberg, B., et al. Mutations in antiquitin in individuals with pyridoxine-dependent seizures. Nat. Med. 12 (2006), 307–309.
8. 8 Farrant, R.D., Walker, V., Mills, G.A., Mellor, J.M., Langley, G.J., Pyridoxal phosphate de-activation by pyrroline-5-carboxylic acid. Increased risk of vitamin B6 deficiency and seizures in hyperprolinemia type II. J. Biol. Chem. 276 (2001), 15107–15116.
9. 9 Ng, B.G., Freeze, H.H., Human genetic disorders involving glycosylphosphatidylinositol (GPI) anchors and glycosphingolipids (GSL). J. Inherit. Metab. Dis. 38 (2015), 171–178.
10. 10 Ikegawa, S., Isomura, M., Koshizuka, Y., Nakamura, Y., Cloning and characterization of human and mouse PROSC (proline synthetase co-transcribed) genes. J. Hum. Genet. 44 (1999), 337–342.
11. 11 Ito, T., Iimori, J., Takayama, S., Moriyama, A., Yamauchi, A., Hemmi, H., Yoshimura, T., Conserved pyridoxal protein that regulates Ile and Val metabolism. J. Bacteriol. 195 (2013), 5439–5449.
12. 12 Prunetti, L., El Yacoubi, B., Schiavon, C.R., Kirkpatrick, E., Huang, L., Bailly, M., ElBadawi-Sidhu, M., Harrison, K., Gregory, J.F., Fiehn, O., et al. Evidence That COG0325 Proteins are involved in PLP Homeostasis. Microbiology 162 (2016), 694–706.
13. 13 Li, H., Durbin, R., Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25 (2009), 1754–1760.
14. 14 McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S., Daly, M., DePristo, M.A., The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20 (2010), 1297–1303.
15. 15 Wang, K., Li, M., Hakonarson, H., ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res., 38, 2010, e164.
16. 16 Footitt, E.J., Clayton, P.T., Mills, K., Heales, S.J., Neergheen, V., Oppenheim, M., Mills, P.B., Measurement of plasma B6 vitamer profiles in children with inborn errors of vitamin B6 metabolism using an LC-MS/MS method. J. Inherit. Metab. Dis. 36 (2013), 139–145.
17. 17 Albersen, M., Bosma, M., Jans, J.J., Hofstede, F.C., van Hasselt, P.M., de Sain-van der Velden, M.G., Visser, G., Verhoeven-Duif, N.M., Vitamin B6 in plasma and cerebrospinal fluid of children. PLoS ONE, 10, 2015, e0120972.
18. 18 Albersen, M., Groenendaal, F., van der Ham, M., de Koning, T.J., Bosma, M., Visser, W.F., Visser, G., de Sain-van der Velden, M.G., Verhoeven-Duif, N.M., Vitamin B6 vitamer concentrations in cerebrospinal fluid differ between preterm and term newborn infants. Pediatrics 130 (2012), e191–e198.
19. 19 Pons, R., Ford, B., Chiriboga, C.A., Clayton, P.T., Hinton, V., Hyland, K., Sharma, R., De Vivo, D.C., Aromatic L-amino acid decarboxylase deficiency: clinical features, treatment, and prognosis. Neurology 62 (2004), 1058–1065.
20. 20 Vistoli, G., De Maddis, D., Straniero, V., Pedretti, A., Pallavicini, M., Valoti, E., Carini, M., Testa, B., Aldini, G., Exploring the space of histidine containing dipeptides in search of novel efficient RCS sequestering agents. Eur. J. Med. Chem. 66 (2013), 153–160.
21. 21 Whyte, M.P., Mahuren, J.D., Fedde, K.N., Cole, F.S., McCabe, E.R., Coburn, S.P., Perinatal hypophosphatasia: tissue levels of vitamin B6 are unremarkable despite markedly increased circulating concentrations of pyridoxal-5′-phosphate. Evidence for an ectoenzyme role for tissue-nonspecific alkaline phosphatase. J. Clin. Invest. 81 (1988), 1234–1239.
22. 22 Phillips, R.S., Chemistry and diversity of pyridoxal-5′-phosphate dependent enzymes. Biochim. Biophys. Acta 1854 (2015), 1167–1174.
23. 23 Kajita, R., Goto, T., Lee, S.H., Oe, T., Aldehyde stress-mediated novel modification of proteins: epimerization of the N-terminal amino acid. Chem. Res. Toxicol. 26 (2013), 1926–1936.
24. 24 Terzuoli, L., Leoncini, R., Pagani, R., Guerranti, R., Vannoni, D., Ponticelli, F., Marinello, E., Some chemical properties and biological role of thiazolidine compounds. Life Sci. 63 (1998), 1251–1267.
25. 25 Schonbeck, N.D., Skalski, M., Shafer, J.A., Reactions of pyrzdoxal 5′-phosphate, 6-aminocaproic acid, cysteine, and penicilamine. Models for reactions of Schiff base linkages in pyridoxal 5′-phosphate-requiring enymes. J. Biol. Chem. 250 (1975), 5343–5351.
26. 26 Eswaramoorthy, S., Gerchman, S., Graziano, V., Kycia, H., Studier, F.W., Swaminathan, S., Structure of a yeast hypothetical protein selected by a structural genomics approach. Acta Crystallogr. D Biol. Crystallogr. 59 (2003), 127–135.
27. 27 Mills, P.B., Footitt, E.J., Mills, K.A., Tuschl, K., Aylett, S., Varadkar, S., Hemingway, C., Marlow, N., Rennie, J., Baxter, P., et al. Genotypic and phenotypic spectrum of pyridoxine-dependent epilepsy (ALDH7A1 deficiency). Brain 133 (2010), 2148–2159.
28. 28 van Karnebeek, C.D., Tiebout, S.A., Niermeijer, J., Poll-The, B.T., Ghani, A., Coughlin, C.R. 2nd, Van Hove, J.L., Richter, J.W., Christen, H.J., Gallagher, R., et al. Pyridoxine-Dependent Epilepsy: An Expanding Clinical Spectrum. Pediatr. Neurol. 59 (2016), 6–12.
29. 29 Hatch, J., Coman, D., Clayton, P., Mills, P., Calvert, S., Webster, R.I., Riney, K., Normal Neurodevelopmental Outcomes in PNPO Deficiency: A Case Series and Literature Review. JIMD Rep. 26 (2016), 91–97.
30. 30 Hoffmann, G.F., Schmitt, B., Windfuhr, M., Wagner, N., Strehl, H., Bagci, S., Franz, A.R., Mills, P.B., Clayton, P.T., Baumgartner, M.R., et al. Pyridoxal 5′-phosphate may be curative in early-onset epileptic encephalopathy. J. Inherit. Metab. Dis. 30 (2007), 96–99.
31. 31 Wassenberg, T., Willemsen, M.A., Geurtz, P.B., Lammens, M., Verrijp, K., Wilmer, M., Lee, W.T., Wevers, R.A., Verbeek, M.M., Urinary dopamine in aromatic L-amino acid decarboxylase deficiency: the unsolved paradox. Mol. Genet. Metab. 101 (2010), 349–356.
32. 32 di Salvo, M.L., Contestabile, R., Safo, M.K., Vitamin B(6) salvage enzymes: mechanism, structure and regulation. Biochim. Biophys. Acta 1814 (2011), 1597–1608.
33. 33 Stepuro, I.I., Solodunov, A.A., Piletskaia, T.P., Iaroshevich, N.A., Ostrovskiĭ, IuM., [Distribution of pyridoxal-5-phosphate between proteins and low molecular weight components of plasma: effect of acetaldehyde]. Ukr. Biokhim. Zh. 60 (1988), 34–41.
34. 34 Bohney, J.P., Fonda, M.L., Feldhoff, R.C., Identification of Lys190 as the primary binding site for pyridoxal 5′-phosphate in human serum albumin. FEBS Lett. 298 (1992), 266–268.
35. 35 Ink, S.L., Henderson, L.M., Effect of binding to hemoglobin and albumin on pyridoxal transport and metabolism. J. Biol. Chem. 259 (1984), 5833–5837.
36. 36 Safo, M.K., Musayev, F.N., Schirch, V., Structure of Escherichia coli pyridoxine 5′-phosphate oxidase in a tetragonal crystal form: insights into the mechanistic pathway of the enzyme. Acta Crystallogr. D Biol. Crystallogr. 61 (2005), 599–604.
37. 37 di Salvo, M.L., Nogués, I., Parroni, A., Tramonti, A., Milano, T., Pascarella, S., Contestabile, R., On the mechanism of Escherichia coli pyridoxal kinase inhibition by pyridoxal and pyridoxal 5′-phosphate. Biochim. Biophys. Acta 1854 (2015), 1160–1166.